Bacterial lipids: Powerful modifiers of the innate immune response

F1000Research

Volumn 6, Issue , 2017, Pages

  Ernst, Robert K ^a   Chandler, Courtney E ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Innate immunity; Lipoproteins; LPS; LTA; TLR2; TLR4

Indexed keywords

BACTERIAL LIPID; FLAGELLIN; LIPID; LIPOPOLYSACCHARIDE; LIPOPROTEIN; LIPOTEICHOIC ACID; NUCLEIC ACID; PEPTIDOGLYCAN; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

BACTERIAL MEMBRANE; BACTERIUM ISOLATION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; IMMUNE EVASION; IMMUNE SYSTEM; IMMUNOSTIMULATION; INNATE IMMUNITY; MEMBRANE VESICLE; NONHUMAN; PATHOGENICITY; REVIEW; UPREGULATION;

EID: 85027258308     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.11388.1     Document Type: Review

References (59)

1. Kawai T Akira S: The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373-84. 20404851 10.1038/ni.1863
2. De Nardo D: Toll-like receptors: Activation, signalling and transcriptional modulation. Cytokine. 2015;74(2):181-9. 25846205 10.1016/j.cyto.2015.02.025
3. Kirschning CJ Schumann RR: TLR2: cellular sensor for microbial and endogenous molecular patterns. Curr Top Microbiol Immunol. 2002;270:121-44. 12467248 10.1007/978-3-642-59430-4_8
4. Lu YC Yeh WC Ohashi PS: LPS/TLR4 signal transduction pathway. Cytokine. 2008;42(2):145-51. 18304834 10.1016/j.cyto.2008.01.006
5. Weidenmaier C Peschel A: Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol. 2008;6(4):276-87. 18327271 10.1038/nrmicro1861
6. Nakayama H Kurokawa K Lee BL: Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 2012;279(23):4247-68. 23094979 10.1111/febs.12041
7. Kovacs-Simon A Titball RW Michell SL: Lipoproteins of bacterial pathogens. Infect Immun. 2011;79(2):548-61. 20974828 10.1128/IAI.00682-10 3028857
8. Mühlradt PF Kiess M Meyer H: Isolation, structure elucidation, and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J Exp Med. 1997;185(11):1951-8. 9166424 10.1084/jem.185.11.1951 2196331
9. Ishikawa E Mori D Yamasaki S: Recognition of Mycobacterial Lipids by Immune Receptors. Trends Immunol. 2017;38(1):66-76. 27889398 10.1016/j.it.2016.10.009
10. Beutler B Jiang Z Georgel P: Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu Rev Immunol. 2006;24:353-89. 16551253 10.1146/annurev.immunol.24.021605.090552
11. Egan AJ Biboy J van't Veer I: Activities and regulation of peptidoglycan synthases. Philos Trans R Soc Lond B Biol Sci. 2015;370(1679): pii: 20150031. 26370943 10.1098/rstb.2015.0031 4632607
12. Kang SS Sim JR Yun CH: Lipoteichoic acids as a major virulence factor causing inflammatory responses via Toll-like receptor 2. Arch Pharm Res. 2016;39(11):1519-29. 27498542 10.1007/s12272-016-0804-y
13. Oliveira-Nascimento L Massari P Wetzler LM: The Role of TLR2 in Infection and Immunity. Front Immunol. 2012;3:79. 22566960 10.3389/fimmu.2012.00079 3342043
14. Zähringer U Lindner B Inamura S: TLR2 - promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology. 2008;213(3-4):205-24. 18406368 10.1016/j.imbio.2008.02.005
15. Kim NJ Ahn KB Jeon JH: Lipoprotein in the cell wall of Staphylococcus aureus is a major inducer of nitric oxide production in murine macrophages. Mol Immunol. 2015;65(1):17-24. 25600878 10.1016/j.molimm.2014.12.016 F1000 Recommendation
16. Kang SS Noh SY Park OJ: Staphylococcus aureus induces IL-8 expression through its lipoproteins in the human intestinal epithelial cell, Caco-2. Cytokine. 2015;75(1):174-80. 25982554 10.1016/j.cyto.2015.04.017 F1000 Recommendation
17. Lund LD Ingmer H Frøkiær H: D-Alanylation of Teichoic Acids and Loss of Poly-N-Acetyl Glucosamine in Staphylococcus aureus during Exponential Growth Phase Enhance IL-12 Production in Murine Dendritic Cells. PLoS One. 2016;11(2):e0149092. 26872029 10.1371/journal.pone.0149092 4752283 F1000 Recommendation
18. Theilacker C Diederich AK Otto A: Enterococcus faecalis Glycolipids Modulate Lipoprotein-Content of the Bacterial Cell Membrane and Host Immune Response. PLoS One. 2015;10(7):e0132949. 26172831 10.1371/journal.pone.0132949 4501811 F1000 Recommendation
19. Martinez de Tejada G Heinbockel L Ferrer-Espada R: Lipoproteins/peptides are sepsis-inducing toxins from bacteria that can be neutralized by synthetic anti-endotoxin peptides. Sci Rep. 2015;5:14292. 26390973 10.1038/srep14292 4585737 F1000 Recommendation
20. Noh SY Kang SS Yun CH: Lipoteichoic acid from Lactobacillus plantarum inhibits Pam2CSK4-induced IL-8 production in human intestinal epithelial cells. Mol Immunol. 2015;64(1):183-9. 25481370 10.1016/j.molimm.2014.11.014 F1000 Recommendation
21. Mayerhofer R Fröhlich EE Reichmann F: Diverse action of lipoteichoic acid and lipopolysaccharide on neuroinflammation, blood-brain barrier disruption, and anxiety in mice. Brain Behav Immun. 2017;60:174-87. 27751870 10.1016/j.bbi.2016.10.011 5419569 F1000 Recommendation
22. Hong YF Lee YD Park JY: Lipoteichoic Acid Isolated from Wei ssella cibaria Increases Cytokine Production in Human Monocyte-Like THP-1 Cells and Mouse Splenocytes. J Microbiol Biotechnol. 2016;26(7):1198-205. 27012236 10.4014/jmb.1601.01047 F1000 Recommendation
23. Wang J Qi L Mei L: C. butyricum lipoteichoic acid inhibits the inflammatory response and apoptosis in HT-29 cells induced by S. aureus lipoteichoic acid. Int J Biol Macromol. 2016;88:81-7. 27020942 10.1016/j.ijbiomac.2016.03.054 F1000 Recommendation
24. Jin MS Kim SE Heo JY: Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell. 2007;130(6):1071-82. 17889651 10.1016/j.cell.2007.09.008 F1000 Recommendation
25. Kang JY Nan X Jin MS: Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity. 2009;31(6):873-84. 19931471 10.1016/j.immuni.2009.09.018
26. Jiménez-Dalmaroni MJ Radcliffe CM Harvey DJ: Soluble human TLR2 ectodomain binds diacylglycerol from microbial lipopeptides and glycolipids. Innate Immun. 2015;21(2):175-93. 24591200 10.1177/1753425914524077 4392886 F1000 Recommendation
27. Wilson MM Bernstein HD: Surface-Exposed Lipoproteins: An Emerging Secretion Phenomenon in Gram-Negative Bacteria. Trends Microbiol. 2016;24(3):198-208. 26711681 10.1016/j.tim.2015.11.006
28. Wang Y Liu Q Chen D: Chlamydial Lipoproteins Stimulate Toll-Like Receptors 1/2 Mediated Inflammatory Responses through MyD88-Dependent Pathway. Front Microbiol. 2017;8:78. 28184217 10.3389/fmicb.2017.00078 5266682
29. Dennehy R Romano M Ruggiero A: The Burkholderia cenocepacia peptidoglycan-associated lipoprotein is involved in epithelial cell attachment and elicitation of inflammation. Cell Microbiol. 2017;19(5):e12691. 27886433 10.1111/cmi.12691 F1000 Recommendation
30. Bhattacharyya S Ghosh SK Shokeen B: FAD-I, a Fusobacterium nucleatum Cell Wall-Associated Diacylated Lipoprotein That Mediates Human Beta Defensin 2 Induction through Toll-Like Receptor-1/2 (TLR-1/2) and TLR-2/6. Infect Immun. 2016;84(5):1446-56. 26930710 10.1128/IAI.01311-15 4862701 F1000 Recommendation
31. Miller SI Ernst RK Bader MW: LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol. 2005;3(1):36-46. 15608698 10.1038/nrmicro1068
32. Park BS Song DH Kim HM: Crystal structure of the human TLR4-human MD-2-E.coli LPS Ra complex;2009. 10.2210/pdb3fxi/pdb
33. Lee JO Kim HM Park BS: Crystal structure of mouse TLR4 and mouse MD-2 complex.2007. 10.2210/pdb2z64/pdb
34. Kim SJ Kim HM: Dynamic lipopolysaccharide transfer cascade to TLR4/MD2 complex via LBP and CD14. BMB Rep. 2017;50(2):55-7. 28115037 10.5483/BMBRep.2017.50.2.011 5342866
35. Scott AJ Oyler BL Goodlett DR: Lipid A structural modifications in extreme conditions and identification of unique modifying enzymes to define the Toll-like receptor 4 structure-activity relationship. Biochim Biophys Acta. 2017; pii: S1388-1981(17)30010-0. 28108356 10.1016/j.bbalip.2017.01.004 5513793
36. Steimle A Autenrieth IB Frick J: Structure and function: Lipid A modifications in commensals and pathogens. Int J Med Microbiol. 2016;306(5):290-301. 27009633 10.1016/j.ijmm.2016.03.001
37. Hellum M Trøseid AS Berg JP: The Neisseria meningitidis lpxL1 mutant induces less tissue factor expression and activity in primary human monocytes and monocyte-derived microvesicles than the wild type meningococcus. Innate Immun. 2017;23(2):196-205. 28024455 10.1177/1753425916684201
38. John CM Phillips NJ Din R: Lipooligosaccharide Structures of Invasive and Carrier Isolates of Neisseria meningitidis Are Correlated with Pathogenicity and Carriage. J Biol Chem. 2016;291(7):3224-38. 26655715 10.1074/jbc.M115.666214 4751370
39. Luan L Patil NK Guo Y: Comparative Transcriptome Profiles of Human Blood in Response to the Toll-like Receptor 4 Ligands Lipopolysaccharide and Monophosphoryl Lipid A. Sci Rep. 2017;7:40050. 28053314 10.1038/srep40050 5215261
40. Malgorzata-Miller G Heinbockel L Brandenburg K: Bartonella quintana lipopolysaccharide (LPS): structure and characteristics of a potent TLR4 antagonist for in-vitro and in-vivo applications. Sci Rep. 2016;6:34221. 27670746 10.1038/srep34221 5037446
41. Flad HD Loppnow H Rietschel ET: Agonists and antagonists for lipopolysaccharide-induced cytokines. Immunobiology. 1993;187:303-16. 10.1016/S0171-2985(11)80346-3
42. Schromm AB Brandenburg K Loppnow H: Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem. 2000;267(7):2008-13. 10727940 10.1046/j.1432-1327.2000.01204.x
43. Pathirana RD Kaparakis-Liaskos M: Bacterial membrane vesicles: Biogenesis, immune regulation and pathogenesis. Cell Microbiol. 2016;18(11):1518-24. 27564529 10.1111/cmi.12658
44. Laughlin RC Alaniz RC: Outer membrane vesicles in service as protein shuttles, biotic defenders, and immunological doppelgängers. Gut Microbes. 2016;7(5):450-4. 27600586 10.1080/19490976.2016.1222345 5046169
45. Kulp A Kuehn MJ: Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163-84. 20825345 10.1146/annurev.micro.091208.073413 3525469
46. Jurkoshek KS Wang Y Athman JJ: Interspecies Communication between Pathogens and Immune Cells via Bacterial Membrane Vesicles. Front Cell Dev Biol. 2016;4:125. 27891500 10.3389/fcell.2016.00125 5104960
47. Vanaja SK Russo AJ Behl B: Bacterial Outer Membrane Vesicles Mediate Cytosolic Localization of LPS and Caspase-11 Activation. Cell. 2016;165(5):1106-19. 27156449 10.1016/j.cell.2016.04.015 4874922 F1000 Recommendation
48. Elhenawy W Bording-Jorgensen M Valguarnera E: LPS Remodeling Triggers Formation of Outer Membrane Vesicles in Salmonella. MBio. 2016;7(4): pii: e00940-16. 27406567 10.1128/mBio.00940-16 4958258 F1000 Recommendation
49. Jung AL Hoffmann K Herkt CE: Legionella pneumophila Outer Membrane Vesicles: Isolation and Analysis of Their Pro-inflammatory Potential on Macrophages. J Vis Exp. 2017; (120). 28287548 10.3791/55146 F1000 Recommendation
50. Nicholas A Jeon H Selasi GN: Clostridium difficile-derived membrane vesicles induce the expression of pro-inflammatory cytokine genes and cytotoxicity in colonic epithelial cells in vitro. Microb Pathog. 2017;107:6-11. 28284851 10.1016/j.micpath.2017.03.006 F1000 Recommendation
51. Ho MH Guo ZM Chunga J: Characterization of Innate Immune Responses of Human Endothelial Cells Induced by Porphyromonas gingivalis and Their Derived Outer Membrane Vesicles. Front Cell Infect Microbiol. 2016;6:139. 27826542 10.3389/fcimb.2016.00139 5078693 F1000 Recommendation
52. Zariri A Beskers J van de Waterbeemd B: Meningococcal Outer Membrane Vesicle Composition-Dependent Activation of the Innate Immune Response. Infect Immun. 2016;84(10):3024-33. 27481244 10.1128/IAI.00635-16 5038073 F1000 Recommendation
53. Jeon H Oh MH Jun SH: Variation among Staphylococcus aureus membrane vesicle proteomes affects cytotoxicity of host cells. Microb Pathog. 2016;93:185-93. 26924795 10.1016/j.micpath.2016.02.014 F1000 Recommendation
54. Raeven RH Brummelman J Pennings JL: Bordetella pertussis outer membrane vesicle vaccine confers equal efficacy in mice with milder inflammatory responses compared to a whole-cell vaccine. Sci Rep. 2016;6:38240. 27905535 10.1038/srep38240 5131296 F1000 Recommendation
55. Choi C Park EC Yun SH: Potential Usefulness of Streptococcus pneumoniae Extracellular Membrane Vesicles as Antibacterial Vaccines. J Immunol Res. 2017;2017: 7931982. 28210633 10.1155/2017/7931982 5292160 F1000 Recommendation
56. Oftung F Korsvold GE Aase A: Cellular Immune Responses in Humans Induced by Two Serogroup B Meningococcal Outer Membrane Vesicle Vaccines Given Separately and in Combination. Clin Vaccine Immunol. 2016;23(4):353-62. 26865595 10.1128/CVI.00666-15 4820518 F1000 Recommendation
57. Choi SJ Kim M Jeon J: Active Immunization with Extracellular Vesicles Derived from Staphylococcus aureus Effectively Protects against Staphylococcal Lung Infections, Mainly via Th1 Cell-Mediated Immunity. PLoS One. 2015;10(9):e0136021. 26333035 10.1371/journal.pone.0136021 4558092 F1000 Recommendation
58. Kuipers K Daleke-Schermerhorn MH Jong WS: Salmonella outer membrane vesicles displaying high densities of pneumococcal antigen at the surface offer protection against colonization. Vaccine. 2015;33(17):2022-9. 25776921 10.1016/j.vaccine.2015.03.010 F1000 Recommendation
59. Lee WH Choi HI Hong SW: Vaccination with Klebsiella pneumoniae-derived extracellular vesicles protects against bacteria-induced lethality via both humoral and cellular immunity. Exp Mol Med. 2015;47:e183. 26358222 10.1038/emm.2015.59 4650931 F1000 Recommendation